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Temperature, Egg Size, and Development of Embryos and Alevins of Five Species of Pacific Salmon: A Comparative Analysis a

Terry D. Beacham & Clyde B. Murray

a

a

Department of Fisheries and Oceans , Biological Sciences Branch, Pacific Biological Station , Nanaimo, British Columbia, V9R 5K6, Canada Published online: 09 Jan 2011.

To cite this article: Terry D. Beacham & Clyde B. Murray (1990) Temperature, Egg Size, and Development of Embryos and Alevins of Five Species of Pacific Salmon: A Comparative Analysis, Transactions of the American Fisheries Society, 119:6, 927-945, DOI: 10.1577/1548-8659(1990)1192.3.CO;2 To link to this article: http:// dx.doi.org/10.1577/1548-8659(1990)1192.3.CO;2

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TRANSACTIONS OF

THE

Volume 119

AMERICAN

FISHERIES

November 1990

SOCIETY

Number 6


Transactions of the American Fisheries Society \ 19:927-945, 1990

Temperature, Egg Size, and Development of Embryos and Alevins of Five Species of Pacific Salmon: A Comparative Analysis TERRY D. BEACHAM AND CLYDE B. MURRAY Department of Fisheries and Oceans, Biological Sciences Branch Pacific Biological Station Nanaimo. British Columbia V9R 5K6, Canada Abstract.—We examined rate of development to alevin hatching and fry emergence, embryo and alevin survival, and alevin and fry size for five Pacific salmon species. There was little difference among values for hatching and emergence time predicted by a modified thermal sums model, power law model (log-inverse Belehradek), or quadratic model. Coho salmon Oncorhynchus kisutch had the fastest rates of development to hatching and emergence of the five species investigated; rankings for the other species depended upon temperature range. Coho salmon embryos had the highest survival rates at low incubation (1.5°C) temperatures. Embryos of pink salmon O. gorbuscha had the lowest survival at temperatures less than 4°C. For all five species, incubation temperature was the more important factor in determining alevin length, and egg size was the more important factor in determining alevin weight. Egg weight was a mayor determinant of fry weight at emergence. Rates of development to hatching and emergence, and alevin and fry size, differed by species in response to changes in temperature. Coho salmon alevins and fry were proportionately larger at 4°C than at 8°C or 12°C, but alevins and fry of pink salmon and chum salmon O. keta were largest at 8°C. Variation in development characters of Pacific salmon reflected adaptations to each species* life history pattern. Variation in life history characters of Pacific salmon can be extensive, both among the five North American species and among spawning populations within species. Spawning time varies among and within species, and spawning times of specific populations are often related to specific water temperatures (Sheridan 1962; Brannon 1987). Embryos and alevins can be exposed to a wide temperature range during development, yet the effect of temperature regime on survival and development to fry emergence remains poorly documented, particularly at low temperatures (Alderdice and Velsen 1978; Crisp 1981, 1988). Water temperature has been the primary factor investigated in development rate studies (Embody 1934; Bailey and Evans 1971; Tang et al. 1987), but egg size (Rombough 1985) and genetic vari-

ation (Beacham 1988) have also been investigat-

ed. Accurate prediction of hatching and emergence times is of practical interest in salmon culture (Rombough 1985), and some attempts have been made for some specific salmonid species (Alderdice and Velsen 1978; Crisp 1981, 1988; Jungwirth and Winkler 1984; Humpesch 1985; Tang et al. 1987; Elliott et al. 1987). Crisp (1988) indicated that the ideal approach would be to establish a set of curves relating times of hatching and emergence to temperature for each salmonid species. This has not yet been done in a systematic manner for Pacific salmon, but we have attempted this task in our study. In our investigations of Pacific salmon development, we examined variation in a number of

927

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BEACHAM AND MURRAY

developmental characters over a wide range of in- 1978; Murray 1980; Crisp 1981; Jungwirth and cubation temperatures from a number of salmon Winkler 1984; Humpesch 1985): populations (Appendix Table A. 1). For this study, log/i - log,/*; we integrated the data from previous studies of (2) Pacific salmon development (compiled by Velsen (3) 1987) with more recent data to compare devel'-c); opment in pink salmon Oncorhynchus gorbuscha, (4) chum salmon O. keta, Chinook salmon O. tshawyIog^> = logî + WogXr - c) + (5) tscha, sockeye salmon O. nerka, and echo salmon log^> = logâ + WogXT" - c) + dS. (6) O. kisutch. We compared a number of models relating hatching and emergence timing to temper- The next two models we investigated were polyature for each species, and related variations in nomial expressions (Bottrell 197S; Tang et al. development among species to life history varia- 1987): tions. We also evaluated the relative influences of iog,D = logî + bio&T + (7) temperature and egg weight variations on varialog^D = lo&a + bT + cT2. (8) tions in alevin and fry length and weight. Finally, the size differences among species in alevin and Our final models were of the logistic or exponenfry were compared with differences among pop- tial type (Alderdice and Velsen 1 978; Kogan 1 984; ulations within species and among temperatures. Kane 1988): + cT); log,D = log/i (9) log,D ae*. (10) Methods


(1)

Hatching and emergence timing. —The data base we used was derived from Velsen (1987), and additional data on hatching and emergence times were obtained from the references in Appendix Table A. 1. Ten models were fitted to the hatching and emergence times for each species. For each model, D was the observed hatching or emergence time after fertilization; T was the observed mean temperature (°Q; S was the timing of spawning in the population (days after January 1); and a, b, c, and d were the constants we obtained from the fitted data. We used hatching and emergence data from both constant and variable incubation regimes. Data were transformed to natural logarithms (base e) in all models. Nonlinear models were fitted by the simplex method of parameter estimation, and the standard deviations of the parameter estimates were calculated as in Mittertreiner and Schnute (1985). The comparison of model performance required that a common data base be used for all models. Because some models (5 and 6) required knowledge of population spawning time, some data for each species were omitted if spawning time was unknown. Data for pink salmon were separated into the brood line of origin (populations spawning in either odd- or even-numbered years), because there are significant differences in developmental characters between pink salmon in the two brood lines (Beacham and Murray 1988). The first six equations we examined were variants of a power law model (Alderdice and Velsen

The goodness of fit of each model was evaluated by examining the residual sum of squares between observed and predicted values. Variation in hatching and emergence times was also analyzed by a two-way analysis of variance (ANOVA); species, temperature, and speciestemperature interaction were the sources of variation in the model. Class width for temperatures was set at 1°C intervals. Embryo and alevin survival.— We derived embryo and alevin survival rates with respect to temperature from the data compiled by Velsen ( 1 987), supplemented by additional sources (Appendix Table A. 1 ). Survival rate data were used only when they were derived from constant-temperature experiments. Unweighted mean survival rates were determined for 0.5°C temperature intervals, and the results were plotted. The lower and upper temperatures at which 50% of embryos died were determined by inspection of the plotted data for each species. The upper and lower temperatures at which 50% of alevins died could not be determined for any species. This occurred because embryos were more sensitive to extreme temperatures during development than were alevins, and the death of embryos resulted in no data for alevins. Alevin and fry size.— Date for predictions of alevin and fry size, given egg size and developmental temperature, were derived from studies conducted in our laboratory (Appendix Table A.1), in which a constant temperature regime was main-

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PACIFIC SALMON DEVELOPMENT

tained during development. When the preserved samples of alevins and fry were measured and weighed, fork length was recorded in our laboratory to the nearest 0. 1 mm, total weight was recorded to the nearest milligram, the yolk was separated from the rest of the body and weighed (mg), and tissue weight was determined by subtraction (total weight - yolk weight). Usually 30 alevins and 30 fry were sampled from each female at each constant temperature, and the means of each character examined were used in subsequent analyses. Because the original data were obtained from samples that had been preserved in 10% formalin, they were transformed to fresh sample length and weights by multiplying preserved, water-hardened egg weight by 0.86, alevin length by 1.03, alevin weight by 0.91, fry length by 1.05, and fry weight by 0.88 (Murray 1980). Four models were fitted to the alevin and fry length data. In all models, L was fork length (mm); T was temperature during development (°Q; W was fresh, water-hardened egg weight (mg); and a, b, c. and d were fitted constants. Temperatures included in the analysis were 1.5°C (coho salmon only); 2°C (coho and sockeye salmon); 4°C, 8°C, and 12°C (all species); and 1 5°C (all species except coho salmon). Data points were lengths and weights of alevins or fry by female at each temperature. The models were log^f +

+ clog,r -I- rf(log,7)2; log,!, = log^z + blagJV + clog.T; L = a + bW + cT + dT\ L = a + bW + cT.

(11) (12) (13) (14)

The fit of each model to the observed data was evaluated by examining the proportion of total variation accounted for (R 2). We examined prediction of alevin and fry weight by models (13) and (14), with weight as the dependent variable. The relative effects of temperature and egg weight variation on subsequent alevin and fry size were investigated with the ANOVA model , + Wt + TW

FIGURE 6.—Length and weight of Pacific salmon alevins and fry at incubation temperatures of 8 and 12°C relative to size at 4°C; size at 4°C is defined as 100%. Data for both brood lines of pink salmon are combined.

Water temperatures after egg fertilization increase in spring-spawning species. In contrast to autumn-spawning Pacific salmonids, springspawning species (rainbow trout O. mykiss, grayling Thymallus thymallus) require fewer thermal units at high incubation temperatures than at low temperatures (Jungwirth and Winkler 1984). As development occurs under a warming temperature regime, increased water temperatures would probably indicate more favorable conditions for enhanced survival, and fry emergence would occur earlier. The differential responses of autumn and spring spawners to changes in water temperature during development likely reflect adaptations to the environmental conditions they encounter during development. Variation among Pacific salmon species was observed in development rate, embryo and alevin survival, and alevin and fry size when the same temperatures occurred during development. Coho salmon had the fastest development rate to hatching and emergence, the highest embryo survival at low temperatures during development, and the largest alevins and fry at 4°C, compared with warmer developmental temperatures. Coho salm-

on are also among the latest spawning of the species examined, and their apparent adaptation to


938

BEACHAM AND MURRAY

low water temperatures during development suggests that the species is adapted to spawning during late autumn and early winter. Pink salmon had relatively slow development rates, the poorest embryo survival at low water temperatures, and small alevins and fry at 4°C, compared with those that developed at 8°C. Pink salmon spawn early in autumn, and again the variation in characters associated with development suggest that the variation reflects adaptation to the species life history pattern. In British Columbia, development to fry emergence generally occurs at mean temperatures of 6°C or less in the natural environment. Coho and chum salmon are the latest-spawning species, and they generally had the fastest rates of development to fry emergence under temperature conditions likely encountered in the natural environment. Because the species showed different trends in emergence timing with respect to changes in development temperature, it seems reasonable to infer that these different trends reflect adaptive variation in the species9 response to environmental temperature during development. Populationspecific differences in development can also exist (Beacham and Murray 1987b; Tang et al. 1987), and populations that spawn in extreme environments can probably be expected to have different rates of development and survival than populations in more moderate environments. For example, chum salmon that spawn in the Yukon River have faster rates of development than comparable populations in British Columbia (Beacham et al. 1988). The development time to hatching has been reported to increase progressively for coho, chum, chinook, pink, and sockeye salmon (levleva 1951; Withlerand Morley 1970; Smirnov 1975; Murray and McPhail 1988). Our study showed that this is true for incubation temperatures above 5°C. At lower temperatures, the relative ranking of the species changes, and development time to hatching is slowest for chinook salmon at temperatures below 3°C The relative development rates among Pacific salmon species depend upon the temperature during development. Size of alevins and fry was clearly influenced by both the temperature experienced during development and the size of eggs from which they originated. We found that egg weight was usually the more important determinant of fry length and certainly of fry weight. Larger alevins and fry are generally derived from larger eggs (Smirnov 1975; Kazakov 1981; Wallace and Aasjord 1984). Size

of salmon alevins and fry may be important in determining subsequent growth and survival (Bams 1969; Fowler 1972), and if there is a fry size at emergence for optimal survival, then the appropriate initial egg weight can be selected and water temperature possibly controlled during development in order to produce fry of the optimum size. A substantial global warming is expected to occur in the next 50-100 years as a result of increased atmospheric levels of carbon dioxide and the subsequent climate change (Wigley et al. 1980; Pittock and Salinger 1982). Coho salmon appear to be the species that would be most significantly affected by such warming. They appear to be adapted for low water temperatures during development, and a trend of increasing temperatures during development would likely influence survival dramatically. Climate change may also reduce summer precipitation in the Pacific northwest portion of North America, and again this could have serious implications for survival of age-0 coho salmon. It might also be expected that the distributions of all species will shift northward. Acknowledgments We are indebted to Frank Velsen for his careful compilation of hatching time and embryo survival data (Velsen 1987), which provided the starting point for our analysis. Wally Earner supervised our previous laboratory analysis of variation in developmental characters of Pacific salmon, and also provided substantial support for the current analysis. The manuscript was substantially improved by the comments of referees and editors.

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velopment in pink (Oncorhynchus gorbuscha) and chum salmon (O. keta) at three different temperatures. Genome 30:89-96. Beacham, T. D., and C. B. Murray. 1985. Effect of female size, egg size, and water temperature on developmental biology of chum salmon (Oncorhynchus keta) from the Nitinat River, British Columbia. Canadian Journal of Fisheries and Aquatic Sciences 42:1755-1765. Beacham, T. D., and C. B. Murray. 1986a. Comparative developmental biology of pink salmon (Oncorhynchus gorbuscha) in southern British Columbia. Journal of Fish Biology 28:233-246. Beacham, T. D., and C. B. Murray. 1986b. Comparative developmental biology of chum salmon (Oncorhynchus keta) from the Fraser River, British Columbia. Canadian Journal of Fisheries and Aquatic Sciences 43:252-262. Beacham, T. D., and C. B. Murray. 1987a. Effects of transferring pink (Oncorhynchus gorbuscha) and

chum salmon (O. keta) embryos at different developmental stages to a low incubation temperature. Canadian Journal of Zoology 65:96-105. Beacham, T. D., and C. B. Murray. 1987b. Adaptive variation in body size, age, morphology, egg size and development biology of chum salmon (Oncorhynchus keta) in British Columbia. Canadian Journal of Fisheries and Aquatic Sciences 44:244-261. Beacham, T. D., and C. B. Murray. 1988. Variation in developmental biology of pink salmon (Oncorhynchus gorbuscha) in British Columbia. Canadian Journal of Zoology 66:2634-2648. Beacham, T. D., and C. B. Murray. 1989. Variation in developmental biology of sockeye salmon (Oncorhynchus nerka) and chinook salmon (Oncorhynchus tshawytscha) in British Columbia. Canadian Journal of Zoology 67:2081-2089. Beacham, T. D., C. B. Murray, and R. E. Withler. 1988. Age, morphology, developmental biology, and biochemical genetic stock identification of Yukon River fall chum salmon (Oncorhynchus keta). U.S. Fish and Wildlife Service Fishery Bulletin 86:663-674. Beacham, T. D., F. C. Withler, and R. B. Morley. 1985. Effect of egg size on incubation time and alevin and fry size in chum salmon (Oncorhynchus keta) and coho salmon (O. kisutch). Canadian Journal of Zoology 63:847-850. Bottrell, H. H. 1975. The relationship between temperature and duration of egg development in some epiphytic Cladocera and Copepoda from the River Thames, Reading, with a discussion of temperature functions. Oecologia (Berlin) 18:63-84. Brannon, E. L. 1987. Mechanisms stabilizing salmonid fry emergence timing. Canadian Special Publication of Fisheries and Aquatic Sciences 96:120124. Crisp, D. T. 1981. A desk study of the relationship between temperature and hatching time for the eggs of five species of salmonid fishes. Freshwater Biology 11:361-368. Crisp, D. T. 1988. Prediction, from temperature, of

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eyeing, hatching and "swim-up" times for salmonid embryos. Freshwater Biology 19:41-48. Disler, N. N. 1953. Ecological and morphological characteristics of the Amur autumn chum salmon (Oncorhynchus keta). Trudy Soveshchanii Ikhtiologicheskoi Komissii Akademii Nauk SSSR 1:354362. Translated from Russian: pages 33-41 in Pacific salmon: selected articles from Soviet periodicals. Israel Program for Scientific Translations, Jerusalem, 1961. Elliott, J. M., U. H. Humpesch,andM. A. Hurley. 1987. A comparative study of eight mathematical models for the relationship between water temperature and hatching time of eggs of freshwater fish. Archiv fur Hydrobiologie 109:257-277. Embody, G. C. 1934. Relation of temperature to the incubation periods of the eggs of four species of trout. Transactions of the American Fisheries Society 64:281-291. Fowler, L. G. 1972. Growth and mortality of fingerUng chinook salmon as affected by egg size. Progressive Fish-Culturist 34:66-69. Garside, E. T. 1966. Effects of oxygen in relation to temperature on the development of embryos of brook trout and rainbow trout. Journal of the Fisheries Research Board of Canada 23:1121-1134. Godin, J.-G. J. 1980. Temporal aspects of juvenile pink salmon (Oncorhynchus keta Walbaum) emergence from a simulated gravel redd. Canadian Journal of Zoology 58:735-744. Gribanov, V. I. 1948. The coho salmon (Oncorhynchus kisutch). A biological sketch. Izvestiya Tikhookeanskogo Nauchno-IssledovateFskogo Instituta Rybnogo Khozyaistva i Okeanografii (TINRO) 28: 43-101. (Fisheries Research Board of Canada Translation Series 370.) Hanamura, N. 1966. Salmon of the North Pacific Ocean. Part HI. A review of the life history of North Pacific salmon. 1. Sockeye salmon in the Far East. International North Pacific Fisheries Commission Bulletin 18:1-27. Heggberget, T. G., and J.C.Wallace. 1984. Incubation of the eggs of Atlantic salmon, Salmo salar, at low temperatures. Canadian Journal of Fisheries and Aquatic Sciences 41:389-391. Heming, T. A. 1982. Effects of temperature on utilization of yolk by chinook salmon (Oncorhynchus tshawytscha) eggs and alevins. Canadian Journal of Fisheries and Aquatic Sciences 39:184-190. Holtby, L. B., T. E. McMahon, and J. C. Scrivener. 1989. Stream temperatures and inter-annual variability in the emigration timing of coho salmon (Oncorhynchus kisutch) smolts and fry, and chum salmon (O. keta) fry from Carnation Creek, British Columbia. Canadian Journal of Fisheries and Aquatic Sciences 46:1396-1405. Humpesch, U. H. 1985. Inter- and intra-specific variation in hatching success and embryonic development of five species of salmonids and Thymol/us thymallus. Archiv fur Hydrobiologie 104:129-144. levleva, M. Ya. 1951. Morphology and rate of embryonic development of Pacific salmon. Izvestiya Ti-


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khookeanskogo Nauchno-IssledovatePskogo Insti- Murray, C. B., and T. D. Beacham. 1987. Effect of tuta Rybnogo Khozyaistva i Okeanografii 34:123varying temperature regimes on the development of 130. Translated from Russian: pages 236-244 in Chinook (Oncorhynchus tshawytscha) and chum Pacific salmon: selected articles from Soviet perisalmon (Oncorhynchus keta) embryos and alevins. odicals. Israel Program for Scientific Translations, Canadian Journal of Zoology 65:2672-2681. Jerusalem, 1961. Murray, C. B., T. D. Beacham, and J. D. McPhail. 1990. Influence of parental stock and incubation temperJungwirth, M., and H. Winkler. 1984. The temperaature on the early development of coho salmon (Onture dependence of embryonic development of corhynchus kisutch) in British Columbia. Canadian grayling (Thymallus thymallus). Danube salmon Journal of Zoology 68:347-358. (Hucho hucho), Arctic char (Salvelinus alpinus) and brown trout (Salmo trutta fario). Aquaculture 38: Murray, C. B., and J. D. McPhail. 1988. Effect of in315-327. cubation temperature on the development of five Kane, T. R. 1988. Relationship of temperature and species of Pacific salmon (Oncorhynchus) embryos time of initial feeding of Atlantic salmon. Progresand alevins. Canadian Journal of Zoology 66:266273. sive Fish-Culturist 50:93-97. Kazakov, R. V. 1981. The effect of the size of Atlantic Pittock, A. B., and J. M. Salinger. 1982. Towards resalmon, Sal mo salar L., eggs on embryos and algional scenarios for a CO2 warmed earth. Climatic Change 4:23-40. evins. Journal of Fish Biology 19:353-360. Kogan, V. A. 1984. Dynamics of change in the tem- Rombough, P. J. 1985. Initial egg weight, time to maximum alevin wet weight, and optimal ponding times perature characteristics of embryos of some salfor chinook salmon (Oncorhynchus tshawytscha). monid fishes. Journal of Ichthyology 24:80-88. Canadian Journal of Fisheries and Aquatic Sciences Kubo, T., Y. Hirano, S. Sano, K. Taguchi, and H. Ka42:287-291. sahara. 1955. On the salmon in waters adjacent to Japan. International North Pacific Fisheries Sato, R. 1980. Variations in hatchability and hatching time, and estimation of heritability for hatching time Commission Bulletin 1:59-92. Kwain, W. 1975. Embryonic development, early among individuals within the strain of coho salmon (Oncorhynchus kisutch). Bulletin of National Regrowth, and meristic variation in rainbow trout (Salmo gairdneri) exposed to combinations of light search Institute of Aquaculture 1:21-28. intensity and temperature. Journal of the Fisheries Satterthwaite, F. E. 1946. An approximate distribution Research Board of Canada 32:397-402. of estimates of variance components. Biometrical Bulletin 2:110-114. Mason, J. C. 1976. Some features of coho salmon, Oncorhynchus kisutch, fry emerging from simulated Shapovalov, L., and W. Berrian. 1940. An experiment redds and concurrent changes in photobehavior. U.S. in hatching silver salmon (O. kisutch) eggs in gravel. Fish and Wildlife Service Fishery Bulletin 74:167Transactions of the American Fisheries Society 69: 135-140. 175. Mclntyre, J. D., and J. M. Blanc. 1973. A genetic anal- Shapovalov, L., and A. C. Taft. 1954. The life histories ysis of hatching time in steelhead trout (Salmo of the steelhead rainbow trout (Salmo gairdneri gairdneri). Journal of the Fisheries Research Board gairdneri) and silver salmon (Oncorhynchus kiof Canada 30:137-139. sutch) with special reference to Waddell Creek, CalMead, R. W., and W. L. Woodall. 1968. Comparison ifornia, and recommendations regarding their manof sockeye salmon fry produced by hatcheries, aragement California Fish and Game Fishery Bulletin tificial channels and natural spawning areas. Inter98. national Pacific Salmon Fisheries Commission Shaw, P. A., and J. A. Magh. 1943. The effect of minProgress Report 20. ing silt on the yield of fry from salmon spawning Mittertreiner, A., and J. Schnute. 1985. Simplex: a beds. California Fish and Game 29:29-41. manual and software package for easy nonlinear pa- Sheridan, W. L. 1962. Relation of stream temperatures rameter estimation and interpretation in fishery reto timing of pink salmon escapements in southeast search. Canadian Technical Report of Fisheries and Alaska. Pages 87-102 in N. J. Wilimovsky, editor. Aquatic Sciences 1384. Symposium on pink salmon. H. R. MacMillan LecMurray, C. B. 1980. Some effects of temperature on tures in Fisheries, Institute of Fisheries, University zygote and alevin survival, rate of development and of British Columbia, Vancouver. size at hatching and emergence of Pacific salmon Silver, S. J., C. E. Warren, and P. Doudoroff. 1963. and rainbow trout. Master's thesis. University of Dissolved oxygen requirements of developing steelBritish Columbia, Vancouver. head trout and chinook salmon embryos at different Murray, C. B., and T. D. Beacham. 1986a. Effect of water velocities. Transactions of the American varying temperature regimes on the development of Fisheries Society 92:327-343. pink salmon (Oncorhynchus gorbuscha) eggs and al- Smirnov,A. I. 1960. The characteristics of the biology evins. Canadian Journal of Zoology 64:670-676. of the production and development of the coho OnMurray, C. B., and T. D. Beacham. 1986b. Effect of corhynchus kisutch (Walbaum). Vestnik Moskovdensity and substrate on the development of chum skogo Universiteta Seriya VI Biologiya 1:9-19. salmon (Oncorhynchus keta) eggs and alevins. Pro(Fisheries Research Board of Canada Translation gressive Fish-Culturist 48:242-249. Series 287.)



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data on median hatching time, mortality and emSmirnov, A. I. 1975. The biology, reproduction and bryonic staging. Canadian Data Report of Fisheries development of the Pacific salmon. IzdateTstvo Moskovskogo Universiteta, Moscow, USSR. (Fishand Aquatic Sciences 626. eries and Marine Service Translation Series 3861.) Wallace, J. C, and D. Aasjord. 1984. An investigation Soin, S. G. 1954. Pattern of development of summer of the consequences of egg size for the culture of chum, masu, and pink salmon. Trudy Soveshchanii Arctic charr, Salvelinus alpinus (L.). Journal of Fish Ikhtiologicheskoi Komissii Akademii Nauk SSSR Biology 24:427-435. 4:144-155. Translated from Russian: pages 42-54 Wigley, T. M. L., P. D. Jones, and P. M. Kelly. 1980. in Pacific salmon: selected articles from Soviet peScenario for a warm, high CO2 world. Nature (Lonriodicals. Israel Program for Scientific Translations, don) 283:17-21. Jerusalem, 1961. Withler, F. C, and R. B. Morley. 1970. Sex-related Tang, J., M. D. Bryant, and EL.Brannon. 1987. Effect parental influence on early development of Pacific of temperature extremes on the mortality and desalmon. Journal of the Fisheries Research Board of Canada 27:2197-2214. velopment rates of coho salmon embryos and alevins. Progressive Fish-Culturist 49:167-174. Received September 6, 1989 Velsen, F. P. J. 1987. Temperature and incubation in Accepted April 17, 1990 Pacific salmon and rainbow trout* compilation of

Appendixes follow

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Appendix: Data Sources and Parameter Estimates

TABLE A. 1.—Sources of data in addition to Velsen's (1987) that were used to analyze embryo survival rates, hatching times, alevin survival rates, and emergence times for five species of Pacific salmon. Data present

Embryo survival

Hatching time

Alevin survival

X X X X X X X

X X X X X X

X X X X X X

X X X X X X X X X

X X X X X X X X X X X X

X X X X X X X X X

Emergence time

Reference


Pink salmon

X X X

X

X

X

X X X

X

X X X X X X X X X X X X

X X X X X X X

Beacham etal. (1985) Beacham and Murray (1985) Beacham and Murray (1986b) Murray and Beacham (1986b) Beacham and Murray (1987a) Murray and Beacham (1987) Beacham and Murray (1987b) Beacham etal. (1988) Murray and McPhail (1988) Kubo etal. (1955)

X X X

X X

Chwn salmon X X

Beacham and Murray (1986a) Murray and Beacham (1986a) Beacham and Murray (1987a) Beacham and Murray (1988) Beacham (1988) Murray and McPhail (1988) Brannon (1987)

Disler(1953) Soin(1954)

X X X

X X

X X X X X X

Chinook salmon X X X X X

Sockeye salmon X X

X X

X X

X X X

Coho salmon X X X

X

X

Murray and Beacham (1987) Beacham and Murray (1989) Murray and McPhail (1988) Rombough(1985) Hemmg(1982) Beacham and Murray (1989) Brannon (1987) Mead and Woodall (1968) Murray and McPhail (1988) Hanamura(1966) Murray and McPhail (1988) Murray etal. (1990) Tang etal. (1987) Shapovalov and Berrian (1940) Shaw and Magh (1943) Gribanov(1948) Ievleva(1951) Shapovalov and Taft (1954) Alien (1957) Smirnov (1960) Murray (1980) Smirnov (1975)

943


TABLE A.2.—Parameter estimates for models (2), (4), (5), and (7) when used to predict hatching times for Pacific salmon. Standard deviations are in parentheses. The values lo&a, b, c, and d are fitted constants in the models. Proportions of total variation accounted for (r2) are also listed. Model

lofcfl

b

2 4 5 7

6.663 (0.03) 7.962 (0.98) 10.746(1.17) 5.153(0.13)

-2.557(0.24) -1.382(0.28) -1.409(0.27) 0.006 (0. 14)

2 4 5 7

6.749 (0.02) 6.375 (0.26) 5.037 (0.68) 5.507 (0.08)

-2.910(0.14) -0.885 (0.08) -0.837 (0.07) -0.397 (0.09)

2 4 5

6.413(0.01) 7.049 (0.20) 7.978 (0.28) 5.600 (0.04)

-1.079(0.06) - 1.209 (0.06) -1.272(0.07) -0.404 (0.05)

7

6.283(0.01) 7.192(0.25) 7.726 (0.54) 5.829 (0.08)

-0.125(0.09) -1.292(0.08) -1.320(0.08) -0.536(0.09)

2 4 5 7

6.240 (0.02) 7.889(0.41) 7.427 (0.80) 5.378 (0.04)

-1.045(0.13) -1.536(0.12) -1.533(0.12) -0.250 (0.05)

2 4 5 7

6.727(0.01) 8.734 (0.73) 9.848 (0.78) 5.379 (0.04)

-2.394(0.10) -1.589(0.20) -1.583(0.18) -0.076(0.05)

c

d

t2

Odd-year pink salmon -5.942(2.53) -6.070(2.50) -0. 194 (0.04)

-0.483(0.13)

0.946 0.948 0.957 0.949


Even-year pink salmon - 1 .850 (0.74) - 1 .444 (0.62) -0.076 (0.02)

0.982 0.982

0.215(0.14)

0.983 0.982

Chum salmon

7

-2.407 (0.42) -2.898(0.46) -0.125 (0.01)

0.985 0.987 -0.127(0.03)

0.988 0.987

Chinook salmon 2 4 5

-2.056(0.55) -2.252(0.60) -0.116(0.02)

-0.078 (0.07)

0.991 0.994 0.994 0.994

Cobo salmon -4.085(0.76) -4.062(0.75) -0. 1 84 (0.02)

0.078(0.12)

0.976 0.982 0.982 0.982

Sockeye salmon -7.067(1.68) -6.834(1.50) -0.185(0.02)

-0.208 (0.08)

0.979 0.985 0.986 0.985

944

BEACHAM AND MURRAY

TABLE A. 3.—Parameter estimates for models (2), (4), (5), and (7) when used to predict fry emergence times for Pacific salmon. Standard deviations are in parentheses. The values lo&a, b, c. and d are fitted constants in the models. Proportions of total variation accounted for (r2) are also listed.


Model

lofcfl

c

b

2 4 5 7

7.190(0.02) 6.233(0.12) 7.243 (0.34) 6.33S (0.09)

OM-year pfak -2.663(0.13) -0.693 (0.04) -0.682 (0.04) -0.768 (0.09)

2 4 5 7

7.339(0.01) 7.231 (0.32) 8.074 (0.50) 5.795 (0.04)

ET••.yttfftakMbMNI -3.755 (0.09) -0.967(0.10) -3.446(0.92) -0.979(0.10) -3.580(0.92) -0.212(0.06) -0.111(0.02)

2 4 5 7

6.982 (0.02) 6.307 (0.20) 8.377 (0.22) 6.341 (0.06)

-1.447(0.10) -0.764 (0.07) -0.851 (0.04) -0.793 (0.08)

2 4 5 7

6.872(0.01) 10.404(1.60) 10.319(1.56) 5.901 (0.17)

-0.332 (0.20) -2.043 (0.43) -1.994(0.40) -0.016(0.18)

2 4 5 7

6.812(0.01) 7.018(0.28) 7.599 (0.80) 5.842 (0.04)

-1.643(0.10) -1.069(0.09) -1.073(0.10) -0.394(0.06)

2 4 5

7.227 (0.01) 7.647(0.31) 9.404 (0.65) 5.970(0.02)

-2.560(0.16) -1.134(0.10) -1.169(0.11) -0.276 (0.02)

d

*

tabBM 0.153(0.37) 0.239(0.32) 0.015(0.02)

-0.039(0.43) -0.657(0.29) 0.007 (0.02) Ckfawok ttbnMi -7.575 (3.20) -7.195(3.01) -0.249 (0.05)

-0.186(0.06)

-0.145(0.06)

-0.318(0.03)

-0.003(0.00)

0.983 0.988 0.990 0.988 0.994 0.994 0.994 0.994 0.973 0.988 0.990 0.988 0.955 0.970 0.971 0.970

CohOttlBMNI

-2.062(0.58) -2.092 (0.60) -0.109(0.02)

-0.098(0.13)

0.978 0.979 0.979 0.979

Socktye salami

7

-3.514(0.72) -3.833(0.82) -0.121(0.01)

-0.289(0.09)

0.968 0.969 0.972 0.969

945


TABLE A.4.—Parameter estimates for model (11) for prediction of length and for model (13) for prediction of weight for alevins and fry of Pacific salmon that were maintained at different constant temperatures during development. Standard errors are in parentheses. The values log^fl, b. c. and d are fined constants for model (11), and a, b. c. and d are fitted constants for model (13).


Salmon species

log*aor